Sponges are capable of rebuilding entire functional organisms from dissociated somatic cells. This feat demands radical cytoskeletal reprogramming whose molecular logic remains obscure. Using the Arctic demosponge , we mapped molecular signatures across free-swimming larvae, sessile adults, and early cell aggregates. Integrating RNA-seq, single-cell deconvolution, DIA-LC-MS proteomics, native complex fractionation, live-cell proteasome imaging, and immunofluorescence, we identified stage-associated profiles of cytoskeletal proteins and post-translational modifications (PTMs). Larvae enrich non-classical myosins (Myosin-9/15) and dynamic microtubules for motility; adults deploy spectrin scaffolds and deacetylated microtubules for stability; cell aggregates shift toward microtubule-based transport with targeted proteolysis and stage-specific PTMs on divergent actin HdA6 and ferritin. Live imaging shows ubiquitin-independent 20S proteasome activity at cell contacts in forming aggregates, while mass spectrometry reveals coordinated methionine oxidation and ubiquitination events coinciding with cytoskeletal remodeling. Although bulk data cannot fully separate cell-type composition from intracellular reprogramming, the multi-layered signatures suggest a tightly regulated, stage-specific program. Together, these findings establish a correlative framework linking cytoskeletal architecture, redox-sensitive PTMs, and proteostasis within sponge development and early reaggregation stage. We propose that conserved structural networks are chemically tuned to enable morphological plasticity in early-branching metazoans - a foundation for future functional studies of multicellular morphogenesis.